Recursive adaptation in action: allochronic isolation and divergence of host-associated populations of Rhagoletis pomonella (Diptera: Tephritidae) following its recent introduction to the western United States

Authors: MATTSSON, MONTE - City Of Portland, Oregon; HOOD, GLEN - Wayne State University; Yee, Wee; DOELLMAN, MEREDITH - University Of Notre Dame; GOUGHNOUR, ROBERT - Washington State University; DRISCOE, AMANDA - University Of Notre Dame; VAN DEXTER, SETH - University Of Notre Dame; BRUZZESE, DANIEL - University Of Notre Dame; TAIT, CHEYENNE - University Of Notre Dame; GLOVER, MARY - University Of Notre Dame; MEYERS, PETE - University Of Notre Dame; RUEDAS, LUIS - Portland State University; FEDER, JEFFREY - University Of Notre Dame

Submitted to: Entomologia Experimentalis et Applicata
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/29/2021
Publication Date: N/A
Citation: N/A

Interpretive Summary: An outstanding issue in the study of insect race formation is recursive adaptive divergence, in which the most recent adaptive episode is defined previously similar cases. In the Pacific Northwest (PNW) of the USA, apple maggot fly is a quarantine pest of apple that serves as an ideal model for testing the existence of this phenomenon. Personnel at the USDA laboratory in Wapato, WA, City of Portland Bureau of Environmental Services, Wayne State University, University of Notre Dame, Washington State University, and Portland State University collected apple fly emergence timing data from different host plants across 25 locations in the Pacific Northwest (PNW) across five years. Results showed that apple-infesting fly populations in the PNW have rapidly and repeatedly shifted their adult emergence timing to infest two novel hawthorn tree hosts with different fruiting time. Results are important in that they suggest apple maggot flies have adaptive memory for emergence times, even following introductions, to rapidly and temporally track fruit development of novel host plants when they arise, thus suggesting recursive adaptive divergence in this flies has and is occurring in the the PNW

Technical Abstract: An outstanding issue in the study of insect host races concerns the idea of ‘recursive adaptive divergence’, whereby adaptation can occur repeatedly across space and/or time, and the most recent adaptive episode is defined by one or more previously similar cases. The host plant shift of the apple maggot fly, Rhagoletis pomonella Walsh (Diptera: Tephritidae, Carpomyiini), from ancestral downy hawthorn (Crataegus mollis [Torr. & A. Gray] Scheele) to introduced, domesticated apple (Malus domestica Borkh.) in the eastern United States (US) has long served as a model study system for investigating ecologically–driven host race formation in phytophagous insect specialists. Here, we report results from an annual geography survey of eclosion time demonstrating a similar ecological pattern among nascent host-associated populations of the fly recently introduced ~40 year ago from its native range in the east into the Pacific Northwest (PNW) region of the US. Specifically, using data collected from 25 locations across five years, we show that apple-infesting fly populations in the PNW have rapidly and repeatedly shifted (and maintained differences in) their adult eclosion life history timing to infest two novel hawthorn hosts with different fruiting phenologies—a native (C. douglasii Lindl.) and an introduced (C. monogyna Jacq.) species—generating partial allochronic reproductive isolation in the process. The shifts in the PNW parallel the classic case of host race formation in the eastern US, but have occurred bi-directionally to two hawthorn species with phenologies slightly earlier (black hawthorn) and significantly later (ornamental hawthorn) than apple across years and sites. Our results imply that R. pomonella both possess and can retain extensive standing variation (i.e., ‘adaptive memory’) in diapause traits, even following introductions, to rapidly and temporally track novel phenological host opportunities when they arise. Thus, “specialized” host races may not constitute evolutionary dead ends. Rather, adaptive phenotypic and genetic memory may carry over from one host shift to the next, repeatedly and recursively facilitating host race formation in phytophagous insects